Ascochlorin is a novel, specific inhibitor of the mitochondrial cytochrome bc1 complex

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1797, Issue 3, 2010, Pages 360-370

  Berry, Edward A ^a   Huang, Li shar ^a   Lee, Dong Woo ^b   Daldal, Fevzi ^b   Nagai, Kazuo ^c   Minagawa, Nobuko ^d  

^a SUNY UPSTATE MEDICAL UNIVERSITY   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c CHUBU UNIVERSITY   (Japan)

^d NIIGATA UNIVERSITY OF PHARMACY AND APPLIED LIFE SCIENCES   (Japan)

Author keywords

Ascochlorin; Cytochrome bc1 complex; Qi site; Qo site; Quinol analog inhibitor

Indexed keywords

4 O CARBOXYMETHYL ASCOCHLORIN; 4 O METHYL ASCOCHLORIN; 4 O NICOTINOYL ASCOCHLORIN; AGENTS AFFECTING METABOLISM; ANTIBIOTIC AGENT; ANTIBIOTIC LL Z1272 EPSILON; ANTIFUNGAL AGENT; ANTIINFECTIVE AGENT; ANTIMYCIN A3; ASCOCHLORIN; ASCOFURANONE; CITRININ; CYTOCHROME B; ENZYME INHIBITOR; FUNICULOSIN; IRON SULFUR PROTEIN; MYXOTHIAZOL; PROTEIN INHIBITOR; STIGMATELLIN; SUPEROXIDE; UBIQUINOL CYTOCHROME C REDUCTASE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DRUG BINDING SITE; DRUG INHIBITION; DRUG ISOLATION; DRUG STRUCTURE; ELECTRON SPIN RESONANCE; ELECTRON TRANSPORT; LIGHT; NONHUMAN; OXIDATION REDUCTION REACTION; PICHIA ANOMALA; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPIRATORY CHAIN; TIME;

ALKENES; ANIMALS; ANTI-BACTERIAL AGENTS; ANTIMYCIN A; CATALYTIC DOMAIN; CATTLE; CHICKENS; CRYSTALLOGRAPHY, X-RAY; CYTOCHROMES B; CYTOCHROMES C; ELECTRON SPIN RESONANCE SPECTROSCOPY; ELECTRON TRANSPORT; ELECTRON TRANSPORT COMPLEX III; MALE; MITOCHONDRIA, LIVER; OXIDOREDUCTASES; PHENOLS; PICHIA; POLYENES; RATS; RATS, WISTAR; RESPIRATION; RHODOBACTER CAPSULATUS; SUPEROXIDES; UBIQUINONE;

ASCOCHYTA; BACTERIA (MICROORGANISMS); BOVINAE; FUNGI; PICHIA ANOMALA; RATTUS; RHODOBACTER CAPSULATUS;

EID: 75649124208     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2009.12.003     Document Type: Article

References (66)

1. Sasaki H., Hosokawa T., Sawada M. Isolation and structure of ascofuranone and ascofuranol, antibiotics with hypolipidemic activity. J. Antibiot. 1973, 26:676-680.
2. Fukai Y., Amino H., Hirawake H., Yabu Y., Ohta N., Minagawa N., Sakajo S., Yoshimoto A., Nagai K., Takamiya S., Kojima S., Kita K. Functional expression of the ascofuranone-sensitive Trypanosoma brucei brucei alternative oxidase in the cytoplasmic membranes of Escherichia coli. Comp. Biochem. Physiol. 1999, C124:141-148.
3. Minagawa N., Yabu Y., Kita K., Nagai K., Ohta N., Meguro K., Sakajo S., Yoshimoto A. An antibiotic, ascofuranone, specifically inhibits respiration and in vitro growth of long slender bloodstream forms of Trypanosoma brucei brucei. Mol. Biochem. Parasitol. 1996, 81:127-136.
4. Nihei C., Fukai Y., Kawai K., Osanai A., Yabu Y., Suzuki T., Ohta N., Minagawa N., Nagai K., Kita K. Purification of active recombinant trypanosome alternative oxidase. FEBS Lett. 2003, 538:35-40.
5. Tamura G., Suzuki S., Takatsuki A., Ando K., Arima K. Ascochlorin, a new antibiotic, found by the paper disc agar-diffusion method. J. Antibiot. 1968, 21:539-544.
6. Takatsuki A., Tamura G., Arima K. Antiviral and antitumor antibiotics. XIV. Effects of ascochlorin and other respiration inhibitors on multiplication of Newcastle disease virus in cultured cells. Appl. Microbiol. 1969, 17:825-829.
7. Nawata Y., Ando K., Tamura G., Arima K., Iitaka Y. The molecular structure of ascochlorin. J. Antibiot. 1969, 22:511-512.
8. Nawata Y., Iitaka Y. The crystal structure of ascochlorin p-bromobenzenesulfonate. Bull. Chem. Soc. Jpn. 1971, 44:2652-2660.
9. Ellestad G.A., Evans R.H., Kunstman M.P. Some new terpenoid metabolites from an unidentified Fusarium species. Tetrahedron 1969, 25:1323-1334.
10. Kosuge Y., Suzuki A., Hirota S., Tamura S. Structure of colletochlorin from Colletotrichum nicotianae. Agric. Biol. Chem. 1973, 37:455-456.
11. Kato A., Ando K., Tamura G., Arima K. Cylindrochlorin, a new antibiotic produced by Cylindrocladium. J. Antibiot. 1970, 23:168-169.
12. Hayakawa S., Minato H., Katagiri K. The ilicicolins, antibiotics from Cylindrocladium ilicicola. J. Antibiot. 1971, 24:653-654.
13. Minato H., Katayama T., Hayakawa S., Katagiri K. Identification of ilicicolins with ascochlorin and LL-Z1272. J. Antibiot. 1972, 25:315-316.
14. Cagnoli-Bellavita N., Ceccherelli P., Fringuelli R., Ribaldi M. Ascochlorin: a terpenoid metabolite from Acremonium luzulae. Phytochemistry 1975, 14:807.
15. Takamatsu S., Rho M.C., Masuma R., Hayashi M., Komiyama K., Tanaka H., Omura S. A novel testosterone 5α-reductase inhibitor, 8'9'-dehydroascochlorin produced by Verticillium sp. FO-2787. Chem. Pharm. Bull. 1994, 42:953-956.
16. Seephonkai P., Isaka M., Kittakoop P., Boonudomlap U., Thebtaranonth Y. A novel ascochlorin glycoside from the insect pathogenic fungus Verticillium hemipterigenum BCC2370. J. Antibiot. 2004, 57:10-16.
17. Che Y., Swenson D.C., Bloer J.B., Koster B., Malloch D. Pseudodestruxins A and B: new cyclic depsipeptides from the coprophilous fungus Nigrosabulum globosum. J. Nat. Prod. 2001, 64:555-558.
18. Singh S.B., Ball R.G., Bills G.F., Cascales C., Gibbs J.B., Goetz M.A., Hoogsteen K., Jenkins R.G., Liesch J.M., Lingham R.B., Silverman K.C., Zink D.L. Chemistry and biology of cylondrols: novel inhibitors of Ras farnesyl-protein transferase from Cylindrocarpon lucidum. J. Org. Chem. 1996, 61:7727-7737.
19. Hosokawa T., Ando K., Tamura G. An ascochlorin derivative, AS-6, reduces insulin resistance in the genetically obese diabetic mouse, db/db. Diabetes 1985, 34:267-274.
20. Hosokawa T., Ando K., Tamura G. Treatment with an ascochlorin derivative, AS-6, increases 45Ca2+ binding on the plasma membrane of adipocytes in db/db mice. Biochem. Biophys. Res. Commun. 1985, 127:247-253.
21. Tsuruga M., Nakajima H., Ozawa S., Togashi M., Chang Y.C., Ando K., Magae J. Characterization of 4-O-methyl-ascochlorin-induced apoptosis in comparison with typical apoptotic inducers in human leukemia cell lines. Apoptosis 2004, 9:429-435.
22. Hong S., Park K.K., Magae J., Ando K., Lee T.S., Kwon T.K., Kwak J.Y., Kim C.H., Chang Y.C. Ascochlorin inhibits matrix metalloproteinase-9 expression by suppressing activator protein-1-mediated gene expression through the ERK1/2 signaling pathway: inhibitory effects of ascochlorin on the invasion of renal carcinoma cells. J. Biol. Chem. 2005, 280:25202-25209.
23. Nakajima H., Mizuta N., Sakaguchi K., Fujiwara I., Mizuta M., Furukawa C., Chang Y.C., Magae J. Aberrant expression of Fra-1 in estrogen receptor-negative breast cancers and suppression of the propagation in vivo by ascochlorin, an antibiotic that inhibits cellular activator protein-1 activity. J. Antibiot. 2007, 60:682-689.
24. Jeong J.H., Nakajima H., Magae J., Furukawa C., Taki K., Otsuka K., Tomita M., Lee I.S., Kim C.H., Chang H.W., Min K.S., Park K.K., Park K.K., Chang Y.C. Ascochlorin activates p53 in a manner distinct from DNA damaging agents. Int. J. Cancer 2009, 124:2797-2803.
25. Mogi T., Ui H., Shiomi K., Omura S., Miyoshi H., Kita K. Antibiotics LL-Z1272 identified as novel inhibitors discriminating bacterial and mitochondrial quinol oxidases. Biochim. Biophys. Acta 2009, 1787:129-133.
26. Mitchell P. Possible molecular mechanisms of the protonmotive function of cytochrome systems. J. Theor. Biol. 1976, 62:267-327.
27. 1 complex. Transport in Bacteria, Mitochondria, and Chloroplasts: Protonmotive Force 1986, 126:253-271. Academic Press Inc., New York. S. Fleischer, B. Fleischer (Eds.).
28. 1 complex. J. Biol. Chem. 2004, 279:8708-8714.
29. 1. Nature 1998, 392:677-684.
30. 1 complex. Science 1998, 281:64-71.
31. 1 complex from bovine heart. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:8026-8033.
32. i site. Biochemistry 2003, 42:9067-9080.
33. Minagawa N., Sakajo S., Komiyama T., Yoshimoto A. Essential role of ferrous iron in cyanide-resistant respiration in Hansenula anomala. FEBS Lett. 1990, 267:114-116.
34. Minagawa N., Koga S., Nakano M., Sakajo S., Yoshimoto A. Possible involvement of superoxide anion in the induction of cyanide-resistant respiration in Hansenula anomala. FEBS Lett. 1992, 203:217-219.
35. Sakajo S., Minagawa N., Yoshimoto A. Characterization of the alternative oxidase protein in the yeast Hansenula anomala. FEBS Lett. 1993, 318:310-312.
36. Sakajo S., Minagawa N., Komiyama T., Yoshimoto A. Molecular cloning of cDNA for antimycin A-inducible mRNA and its role in cyanide-resistant respiration in Hansenula anomala. Biochim. Biophys. Acta 1991, 1090:102-108.
37. Minagawa N., Koga S., Nakano M., Sakajo S., Yoshimoto A. Generation of superoxide anion detected by chemiluminescence method in the cyanide-sensitive mitochondria and the induction of cyanide-resistant respiration in the yeast, Hansenula anomala. Oxygen Radicals 1992, 203-206. Elsevier Science B. V., Amsterdam. K. Yagi, M. Kondo, E. Niki, T. Yoshikawa (Eds.).
38. Trumpower B.L., Edwards C.A. Purification of a reconstitutively active iron-sulfur protein (oxidation factor) from succinate•cytochrome c reductase complex of bovine heart mitochondria. J. Biol. Chem. 1979, 254:8697-8706.
39. Johnson D., Lardy H. Isolation of liver or kidney mitochondria. Oxidation and Phosphorylation 1967, 10:94-96. Academic Press Inc., New York. R.W. Estabrook, M.E. Pullman (Eds.).
40. 1 complex and for photosynthetic growth of Rhodobacter capsulatus. Proc. Natl. Acad. Sci. U. S. A. 1991, 88:492-496.
41. o site occupants and the head domain position of the Fe-S protein subunit. Biochem 2004, 43:2217-2227.
42. 1-cy fusion complexes reveal the distance constraints for functional electron transfer between photosynthesis components. J. Biol. Chem. 2008, 283:13973-13982.
43. 1 complex. Biochemistry 1995, 34:16004-16012.
44. Roberson D.E., Dutton P.L. The nature and magnitude of the charge-separation reactions of ubiquinol cytochrome c2 oxidoreductase. Biochim. Biophys. Acta 1988, 935:273-291.
45. Dutton P.L. Redox potentiometry: determination of midpoint potentials of oxidation-reduction components of biological electron-transfer systems. Methods Enzymol. 1978, 54:411-435.
46. Sternberg J., Stillo H., Schwendeman R. Spectrophotometric analysis of multicomponent systems using the least squares method in matrix form. Anal. Chem. 1960, 32:84-90.
47. 1 complex from potato tuber mitochondria, J. Biol. Chem. 1991, 266:9064-9077.
48. 1 complex. J. Biol. Chem. 2008, 283:21649-21654.
49. Duel D.H., Thorn M.B. Effects of 2,3-dimercaptopropanol and antimycin on absorption spectra of heart-muscle preparations. Biochim. Biophys. Acta 1962, 59:426-436.
50. 1 complex. J. Biol. Chem. 2004, 279:15040-15049.
51. von Jagow G., Engel W.D. Complete inhibition of electron transfer from ubiquinol to cytochrome b by the combined action of antimycin and myxothiazol. FEBS Lett. 1981, 136:19-24.
52. 1-site electron transfer inhibitors on the absorption spectra of mitochondrial cytochrome b. FEBS Lett. 1985, 181:95-99.
53. o site inhibitor bound. J. Biol. Chem. 2003, 278:31303-31311.
54. Auffinger P., Hays F.A., Westhof E., Ho P.S. Halogen bonds in biological molecules. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:16789-16794.
55. Berry E.A., Zhang Z., Huang L.S., Kim S.H. Structures of Quinone binding sites in bc complexes: functional implications. Biochem. Soc. Trans. 1999, 27:565-572.
56. 1 complex from the yeast Saccharomyces cerevisiae co-crystallized with an antibody Fv fragment. Structure 2000, 8:669-684.
57. 1 complex: a new crystal structure reveals an altered intramolecular hydrogen-bonding pattern. J. Mol. Biol. 2005, 351:573-597.
58. Maklashina E., Cecchini G. Comparison of catalytic activity and inhibitors of quinone reactions of succinate dehydrogenase and fumarate reductase from Escherichia coli. Arch. Biochem. Biophys. 1999, 369:223-232.
59. Svensson-Ek M., Brzezinski P. Oxidation of ubiquinol by cytochrome bo3 from Escherichia coli: kinetics of electron and proton transfer. Biochem 1997, 36:5425-5431.
60. Yeh J.I., Chinte U., Du S. Structure of glycerol-3-phosphate dehydrogenase, an essential monotopic membrane enzyme involved in respiration and metabolism. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:3280-3285.
61. Lam E. The effects of quinone analogues on cytochrome b6 reduction and oxidation in a reconstituted system. FEBS Lett. 1984, 172:255-260.
62. Tsai A.L., Kauten R., Palmer G. The interaction of yeast complex III with some respiratory inhibitors. Biochim. Biophys. Acta 1985, 806:418-426.
63. i sites and the heme prosthetic groups in ubiquinol-cytochrome c oxidoreductase. Biochem. 1993, 32:11162-11172.
64. Degli Esposti M., Ghelli A., Crimi M., Baracca A., Solaini G., Tron T., Meyer A. Cytochrome b of fish mitochondria is strongly resistant to funiculosin, a powerful inhibitor of respiration. Arch. Biochem. Biophys. 1992, 295:198-204.
65. Jones T.A., Zhou J.Y., Cowan S.W., Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors on these models. Acta Crystallogr. 1991, A47:110-119.
66. Ponder J.W., Richards F.M. Tertiary templates for proteins: use of packing criteria in the enumeration of allowed sequences for different structural classes. J. Mol. Biol. 1987, 193:775-791.